A new species of from the Amazon Author(s): Mario A. Cozzuol , Camila L. Clozato , Elizete C. Holanda , Flávio H. G. Rodrigues , Samuel Nienow , Benoit de Thoisy , Rodrigo A. F. Redondo , and Fabrício R. Santos Source: Journal of Mammalogy, 94(6):1331-1345. 2013. Published By: American Society of Mammalogists DOI: http://dx.doi.org/10.1644/12-MAMM-A-169.1 URL: http://www.bioone.org/doi/full/10.1644/12-MAMM-A-169.1

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BioOne sees sustainable scholarly publishing as an inherently collaborative enterprise connecting authors, nonprofit publishers, academic institutions, research libraries, and research funders in the common goal of maximizing access to critical research. Journal of Mammalogy, 94(6):1331–1345, 2013

A new species of tapir from the Amazon

MARIO A. COZZUOL,* CAMILA L. CLOZATO,ELIZETE C. HOLANDA,FLA´ VIO H. G. RODRIGUES,SAMUEL NIENOW, BENOIT DE THOISY,RODRIGO A. F. REDONDO, AND FABRICIO´ R. SANTOS* Universidade Federal de Minas Gerais, Avenida Antonio Carlos 6627, Belo Horizonte, Minas Gerais, (MAC, CLC, FHGR, RAFR, FRS) Universidade Federal do Rio Grande do Sul and Funda¸ca˜o Zoobotanicaˆ do Rio Grande do Sul, R. Dr. Salvador Fran¸ca, 1427, Porto Alegre, Rio Grande do Sul, Brazil (ECH) Instituto Pro-Carn´ ´ıvoros, Avenida Hora´cio Neto, 1030, Atibaia, Sa˜o Paulo, Brazil (FHGR) Instituto Chico Mendes de Biodiversidade, Avenida Dr. Mendon¸ca Lima 481, Guajara´-Mirim, Rondoˆnia, Brazil (SN) Kwata NGO & Institut Pasteur de la Guyane, 23 Avenue Pasteur, Cayenne, (BdeT) Institute of Science and Technology, Am Campus 1, 3400, Klosterneuburg, Austria (RAFR) * Correspondents: [email protected], [email protected]

All known species of extant are allopatric: 1 in southeastern Asia and 3 in Central and . The fossil record for tapirs, however, is much wider in geographical range, including Europe, Asia, and North and South America, going back to the late Oligocene, making the present distribution a relict of the original one. We here describe a new species of living Tapirus from the Amazon rain , the 1st since T. bairdii Gill, 1865, and the 1st new Perissodactyla in more than 100 years, from both morphological and molecular characters. It is shorter in stature than T. terrestris (Linnaeus, 1758) and has distinctive skull morphology, and it is basal to the clade formed by T. terrestris and T. pinchaque (Roulin, 1829). This highlights the unrecognized biodiversity in western Amazonia, where the biota faces increasing threats. Local peoples have long recognized our new species, suggesting a key role for traditional knowledge in understanding the biodiversity of the region.

Key words: Amazon, biodiversity, cladistics, genetics, morphometry, new species, Tapirus

Ó 2013 American Society of Mammalogists DOI: 10.1644/12-MAMM-A-169.1

The known living tapirs inhabit southeastern Asia, Central are preferred food for local human populations and are actors in America, and South America (Nowak 1997). Extant tapir the traditional beliefs of Amerindian communities (Nowak diversity and distribution are relicts of a richer group of species 1997; International Union for the Conservation of Nature and and larger distribution range attained during the Pleistocene Natural Resources 2009). (Simpson 1945; Nowak 1997; Hulbert 1999; Holanda et al. Here we describe a 5th living species of Tapirus, the 4th in 2011). Despite some controversies (Hershkovitz 1954), the 4 the Neotropics, the 1st since T. bairdii Gill, 1865, one of the living and many fossil species from Eurasia and the Americas largest land recently described, and the only new are all placed in the genus Tapirus (Simpson 1945; Perissodactyla in more than 100 years (Ceballos and Ehlrich Hershkovitz 1954; Yingjun and Gaunfu 1987; Hulbert 1999; 2009). Despite popular accounts of the occurrence of more than Spassov and Ginsburg 1999; Holanda and Cozzuol 2006; 1 tapir species in lowland Amazonia, it was assumed that Ferrero and Noriega 2007; Holanda et al. 2011). Tapirs reached observed diversity of both morphological (Hershkovitz 1954) South America during the Great American Biotic Interchange, and molecular (de Thoisy et al. 2010) characters represented where they survived the late Pleistocene extinction, as the variations of T. terrestris (Linnaeus, 1758). We present here largest living terrestrial on the continent (Woodburne detailed morphological and molecular (mitochondrial DNA 2010). All extant species are currently considered to be [mtDNA]) comparisons of specimens from western Brazilian vulnerable or endangered, by overhunting and habitat destruc- Amazon with all other Tapirus species, which indicate the tion (International Union for the Conservation of Nature and Natural Resources 2009). As seed predators and dispersers, they have key roles in the dynamics of rain , , Pantanal, and high mountain ecosystems (Olmos 1997). They www.mammalogy.org 1331 1332 JOURNAL OF MAMMALOGY Vol. 94, No. 6 presence of this new taxon. Our study includes the largest Molecular phylogenetic analyses.—The following total geographic sampling of T. terrestris so far attempted. sample numbers, or sequences, or both, were included in the analyses: T. terrestris: n ¼ 52, T. bairdii: n ¼ 3, T. pinchaque: n ¼ 5, T. indicus: n ¼ 4, Tapirus sp. nov.: n ¼ 4. caballus MATERIALS AND METHODS or Rhinocerotidae, or both, were used as out-groups. Samples.—Skull samples and measures were obtained from The DNA sequences from 3 mtDNA genes (cytochrome b specimens in museum collections, those collected in the field, [Cytb], cytochrome oxidase I [COI], and cytochrome oxidase II or provided by indigenous hunters. Skull and tissue [COII]) from living Tapirus species were generated and samples obtained from collected specimens in Brazil were compared to previously published data (Ashley et al. 1996; approved by Ministerio´ do Meio Ambiente, Sistema de Norman and Ashley 2000; de Thoisy et al. 2010). We included Autoriza¸ca˜o e Informa¸ca˜o em Biodiversidade—SISBIO a thorough analysis of the Cytb in a large geographic sampling (number: 21055-2; issue date: 11 December 2009). No in South America, such as has been shown to be useful in permit was required for field sampling carried out in French recovering mammalian phylogeny and exposing cryptic species Guiana. A sample of Tapirus indicus, Desmarest, 1819, was (Baker and Bradley 2006; Redondo et al. 2008). Sequence provided by the San Diego Zoo, San Diego, California. alignments were performed using Clustal W 2.1 (Larkin et al. Sequence data for other specimens and species from different 2007) and edited or concatenated, or both, when necessary with countries were retrieved from GenBank (Benson et al. 2005), the Alignment Explorer function implemented in MEGA 5.1 or published elsewhere (de Thoisy et al. 2010). (Tamura et al. 2011). The resulting alignments were used in Morphological studies.—Canonical variate analysis phylogenetic reconstructions by 2 methods. First, a maximum- (multivariate analysis of variance [MANOVA]–canonical likelihood search was performed in PhyML 3.0.1 (Guindon et variate analysis [CVA]) of 22 cranial measurements al. 2010) using the GTRþCþinv model with parameters (Supporting Information S1, DOI: 10.1644/ estimated from the data by the maximum-likelihood approach. 12-MAMM-A-169.S1) was performed with the software The initial tree was a BioNJ tree and the search was performed PAST version 2.14 (Hammer et al. 2001), using the using both NNI and SPR rearrangements in each interaction Hotelling’s Bonferroni-corrected option to test the keeping only the tree with best likelihood score. After a full discrimination of each of the species. Data were available for PhyML search on tree topology and parameters, the maximum- likelihood tree was used again as an initial tree for a new run all living species: T. terrestris: n ¼ 52, T. indicus: n ¼ 3, T. and the search was repeated until no significant gain in bairdii: n ¼ 4, T. pinchaque (Roulin, 1829): n ¼ 3, Tapirus sp. likelihood was observed in a likelihood-ratio test. The nov.: n ¼ 8 (for a list of the specimens see Supporting confidence in the clades was assessed through the approximate Information S2, DOI: 10.1644/12-MAMM-A-169.S2). Some likelihood-ratio (aLRT) test (Anisimova and Gascuel 2006; fossil species were included, which represent all of the South Anisimova et al. 2011). Second, we used a Bayesian inference American and several North American taxa known from skulls method with MrBayes 3.2.1 (Ronquist et al. 2011) using a complete enough to take most, if not all, the measurements GTRþCþinv model of nucleotide evolution and assuming flat used. Although some skulls of Tapirus sp. nov. collected by Dirichlet priors for parameter estimates and unconstrained the Karitiana Indians were partially damaged, so some branch lengths. The search was carried out using 2 independent measurements are missing, they were included in some of the runs of 4 Markov chains (1 cold and 3 heated) for 3 3 106 analyses. Qualitative comparison of discrete characters was generations, sampling every 300 generations with a burn-in of derived from available specimens, museum collections, and the 25% of the samples for the estimates of topology and literature. A figure including the measurements, their parameters. Stationarity of the chains was checked by plotting descriptions, and a list of specimens used in the analyses are parameters against generation in Tracer 1.5 (Rambaut and provided in Supporting Information S1 and S2. Drummond 2007). Morphological cladistic analysis was performed using TNT We also carried out phylogenetic reconstructions based on version 1.1 (Goloboff et al. 2008) to infer phylogenetic maximum-parsimony criteria for the Cytb data set using the relationships of the tapirs using parsimony with the script software TNT. Additionally, we used the algorithm Median- aquickie.run, provided with the TNT package. The matrix (see Joining (Bandelt et al. 1999), as implemented in the software Supporting Information S3, DOI: 10.1644/12-MAMM-A-169. Network 4.6 (Fluxus Technology Ltd., Suffolk, England), to S3) included 15 taxa and 60 cranial, dental, and postcranial build a Cytb haplotype network to infer all the most- characters, modified from Hulbert and Wallace (2005), with parsimonious relationships among haplotypes, which allowed characters treated as unordered (the character list is shown in the inclusion of multiple allele states and observation of Supporting Information S4, DOI: 10.1644/12-MAMM-A-169. homoplastic reticulations. S4). The in-group included all known living species and 6 Divergence times.—Two methods were used to estimate fossil Tapirus from the Miocene to the Pleistocene of North divergence times among the Tapirus lineages. In the 1st, we and South America. Out-groups included the extinct genera used the Linetree method of Takezaki–Rzhetsky–Nei (Tamura Plesiotapirus and Paratapirus, following previous propositions et al. 2007), which assumes a strict molecular clock. We (Hulbert 1999). assumed an evolutionary substitution rate of 2.5% per million December 2013 COZZUOL ET AL.—NEW AMAZON TAPIR 1333

years (Nabholz et al. 2008). Furthermore we used estimated dates from the fossil record to calibrate the molecular clock and set boundaries in some of the clade splits on the tree to refine the estimates (see Hulbert 1999; Spassov and Ginsburg 1999; Holanda and Cozzuol 2006; Ferrero and Noriega 2007; Holanda et al. 2011; and the morphological analysis below). These age boundaries determined by fossil dates were set in the split between the Asian and American tapirs (15 6 SD 5 million years ago [mya]), for the divergence between T. bairdii and the South American tapirs (7.5 6 1 mya), and also the diversification of South American tapirs (0.13 6 0.1 mya). In a 2nd method, we used a Bayesian estimation implemented in BEAST 1.5.3 (Drummond et al. 2007), with a relaxed molecular clock using the same fossil calibrations above to set the means and standard deviations of a normal distribution used as prior probabilities for the nodes’ ages (Drummond and Rambaut 2006). We also used a strict clock model without constraints on the divergence times of the nodes, with the evolutionary rate described above (2.5%). All estimates were congruent. We have deposited all newly generated sequences in GenBank and the COI sequences of all Tapirus species in the Barcodes of Life Database (Ratsinagan and Hebert 2007). GenBank accession numbers for sequences generated in this work are GU593658–GU593682 and GU737551–GU737565. Details can be found in Supporting Information S5 (DOI: 10.1644/12-MAMM-A-169.S5).

RESULTS Tapirus kabomani, new species Etymology.—Arabo kabomani signifies tapir in the Paumar´ı native language from southern Amazonas, Brazil, where the holotype was collected in December 2009. Holotype.—Universidade Federal de Minas Gerais (UFMG) 3177, a complete skeleton and parts of the skin of a young adult male, with complete fused epiphyses in long bones, but with 3rd molars unerupted (Figs. 1a–e). This specimen has the long-bone epiphyses and vertebral disks fused, indicating physical maturity, although tooth-eruption is incomplete. Tapirs with M1 erupted are already sexually mature and the skull and size subsequently changes little or not at all. The only significant change after M1 eruption is closure of the sutures (M. A. Cozzuol, pers. obs.). Referred specimens.—UFMG 3176, a skull, ribs, and a vertebra of a young adult male (2nd molars unerupted), hunted a few months before collection at 8811013.200 S, 65841041.200 W. Universidade Federal de Rondonia (UNIR-M21); a skull of a mature adult, sex unknown (3rd molars in use) with indication of being shot, from the right margin of the , a few kilometers north of Porto Velho, Rondoˆnia, Brazil (8838008.300 S, 6385300000 W). Six partial skulls (UFMG 3178– FIG.1.—Skull and mandible of the holotype of Tapirus kabomani 3183), hunted by Karitiana Indians in their territory, Rondoˆnia, sp. nov., UFMG 3177. a) Skull, left lateral view; b) mandible, left Brazil, and donated by them to one of us (SN). American lateral view; c) skull, dorsal view; d) skull, ventral view; e) mandible, Museum of Natural History (AMNH) 36661, partial skull and occlusal view. White bar ¼ 5 cm. skin of an adult young male, collected by 1334 JOURNAL OF MAMMALOGY Vol. 94, No. 6

FIG.2.—Map for the known localities of Tapirus kabomani sp. nov. Circle ¼ collected specimens; diamond ¼ DNA inference; triangle ¼ photographs. in January 1912, in Porto Campo at Sepotuba River, Mato nasals, extending up to the frontal–parietal suture; from T. Grosso, Brazil. pinchaque by the gently inclined sagittal crest rising posteriorly Type locality.—Southern Amazonas, Brazil, near BR 319 instead of parallel to the toothrow; from T. bairdii and T. Highway, about 90 km north from Porto Velho, Rondoˆnia, indicus by having a single narrow sagittal crest; from T. Brazil (8807045.7300 S, 63842009.6400 W; Fig. 2). pinchaque, T. terrestris, T. bairdii, and T. indicus by a Distribution.—The new species is present in Amazonas, shallower and less dorsally extended meatal diverticulum fossa, Rondoˆnia, and states in Brazil and in Amazonas and generally smaller size. It differs from all living species plus Department in . The habitats in the localities where the extinct T. webbi, T. veroensis, T. johnsoni,andT. the species was recorded so far are mosaics of forest and open cristatellus by its relatively short limbs (femur length shorter savanna. Local people’s knowledge and photographic than dentary length). Molecularly, the 4 samples of T. documents also suggest that it may be present in the eastern kabomani analyzed shared 7 unambiguous apomorphic Amazon along the Guiana Shield (Amapa´ in Brazil and characters in mtDNA Cytb (960 base pairs [bp]), COI (650 southern French Guiana; Fig. 2). bp), and COII (642 bp) genes, compared with T. indicus, T. Diagnosis.—Tapirus kabomani is the smallest living tapir, bairdii, T. pinchaque,andT. terrestris. The following with total length 130 cm, height at shoulder 90 cm, and body autapomorphic characters define T. kabomani: position 620 mass estimated at about 110 kg. Externally, it differs from the in the Cytb gene (homoplasically present in an individual of T. sympatric T. terrestris by darker hair, lower mane, broader terrestris as shown by the parsimony reconstruction), position forehead, and smaller size; cranially, it differs from T. indicus 401 and 413 of the COI gene, and positions 254, 329, 389, and because the maxillary–premaxillary suture ends anterior to the 395 of the COII gene. T. kabomani also is defined by absence canine; from T. bairdii by the absence of an ossified nasal of 3 synapomorphic positions (302, 401, and 497 of the Cytb septum and dorsal maxillary flanges; from T. terrestris by a gene) that unite the clade T. pinchaque–T. terrestris (see lower sagittal crest, frontals broad and inflated behind the Supporting Information S5 for GenBank accession numbers). December 2013 COZZUOL ET AL.—NEW AMAZON TAPIR 1335

1872, from Pernambuco, Brazil, T. brasiliensis Liais, 1872, from Minas Gerais, Brazil, and T. anulipes Hermann, 1924, from Mato Grosso, Brazil, also have no designated holotypes and cannot be assigned. All of these should be considered as nomina dubia. Tapirus aenigmaticus Gray, 1872, from Macas, eastern Ecuador, was considered by Hershkovitz (1954) to be a young T. terrestris, based on its immature skull, despite that its associated skin supposedly showed characteristics that appear closer to some juveniles of T. pinchaque. As Hershkovitz (1954:476) noted, Gray’s (1872) revision of tapirs is a ‘‘... confusing and misleading source of information. The work is characterized by numerous typographical errors, misquotations of authors, contradictions, and assumptions derived from specimens mislabeled as to sex and locality and mismatched as regards skins and corresponding osteological material.’’ The skull illustrated by Gray (1872:491) is from a very young and the globular shape of the braincase is most likely due to this condition. Because no sign of a sagittal crest is visible in this specimen, and because in T. terrestris the crest is formed at the fetal stage, it seems most likely that the skull and skin may represent a single individual of T. pinchaque. In fact, the collector of this specimen noted that it was captured along with an adult female that did not separate from it. For obscure reasons, Gray (1872) doubted this assertion, and placed the young animal in a different species than the adult, which he called T. leucogenys. The latter specimen has some character- istic features of T. pinchaque, such as white upper and lower lips, but does not possess all characteristics. In any case, neither the skull nor pelt matches the observed specimens of T. FIG.3.—Camera-trap photos of 2 specimens of Tapirus kabomani kabomani. However, in our analysis some DNA sequences in the type locality (southern Amazonas State from Brazil). a) Lateral from the lower cordillera in Ecuador were closer to T. view of the head and anterior body of a male (right) and female (left) specimens. b) Posterior view of the same specimens in the same pinchaque than to other T. terrestris (see Genetic Evidence locality and day, female (left) and male (right). Note the lighter section). The possibility should be pursued that those samples colored patch on lower head and neck of the female. may represent animals like the one described as T. leucogenys. Tapirus ecuadorensis Gray, 1872, from Macas, eastern Ecuador, was based on a juvenile skin. Hershkovitz (1954:485) Potential synonyms.—Many names have been proposed for states that ‘‘Descriptions of species based on skins of striped putative taxa of the genus Tapirus from South America juveniles (T. aenigmaticus, T. ecuadorensis, T. peruvianus) (Hershkovitz 1954), and possibly 1 or more of those names and young adults with persistent juvenile striping (T. anulipes) refer to the species we are describing here. are trivial.’’ Our search of photographic material, zoo Several early names were proposed as substitutes for the specimens, and consultation with colleagues uncovered no original Linnean name, Hippopotamus terrestris, or were work available on intraspecific and interspecific variation of independent descriptions of the same species, and thus are young pelts in tapirs. Gray used few specimens to make his objective synonyms of T. terrestris (Linnaeus, 1758), type observations, giving it an unjustified taxonomic value. The locality Pernambuco, Brazil. In this category are included skins are now more than 150 years old, and curatorial Hydrochaerus tapir Erxleben, 1777, Tapir suillus Blumen- procedures at that time included formalin and arsenic as bach, 1779, and Tapir americanus Gmelin, 1788, from preservatives, which preclude DNA extraction and analyses by Suriname; Tapir anta Zimmermann, 1780, from Pernambuco, current methods. Brazil; and T. tapirus Merriam, 1895. No types are available Tapirus rufus Fisher, 1814, probably from French Guiana, for these names. was based on a skin and a skull, but efforts to locate the Tapirus terrestris has no originally designated holotype and specimen in the institution where it was deposited have been its type locality is Pernambuco, Brazil (Linnaeus, 1758). unsuccessful, and it is assumed lost. Other names proposed for putative new species, including T. The type of T. laurillardi Gray, 1867, without precise type maypuri Roulin, 1829, from the Guianas, T. sabatyra Liais, locality, based on an adult skull, we ascribe to T. terrestris 1336 JOURNAL OF MAMMALOGY Vol. 94, No. 6

FIG.4.—Comparison of the skull of Tapirus kabomani (left, holotype) and T. terrestris (right, Museu de Cienciasˆ Naturais, Pontif´ıcia Universidade Catolica´ de Minas Gerais, Belo Horizonte, Minas Gerais, Brazil, MCN 2750). Left lateral view (above), dorsal view (below). The most significant differences described in text are indicated. White bar ¼ 5 cm.

(Gray, 1867:882, figure A) because it has a high and very lower jaw to the cheeks and the base of the ears, and extends curved sagittal crest, with origin in the frontals. ventrally to the neck, similar to that of T. bairdii. Males do not Tapirus peruvianus Gray, 1872, from Peruvian Amazon, show this patch and seem to be smaller (Figs. 3a and 3b; was based on a juvenile skin and skull. Despite the inutility of Supporting Information S6 and S7, DOI: 10.1644/ the skin as a character, the skull lacks any indication of a 12-MAMM-A-169.S6 and DOI: 10.1644/12-MAMM-A-169. sagittal crest, which precludes assignment to T. terrestris. S7). The ear tips have a white line as in all Tapirus species. Juveniles of comparable age are still unknown for T. kabomani. Skull.—The sagittal crest is single and narrow, as in T. The morphology of the upper deciduous premolar lacks the terrestris and adults of T. pinchaque, but lower than in the 1st cinguloid shelf of the protocone, like T. pinchaque, but this and higher than in the 2nd. Because only adult specimens are feature is present in T. terrestris and in all the known currently known, we do not know if the sagittal crest occurs in specimens of T. kabomani (Hershkovitz 1954:487). We newborns or if it develops later, as in T. pinchaque (Holbrook therefore identify this specimen as a T. pinchaque. 2002). Unlike the latter, the sagittal crest is not horizontal, We examined the holotype skull of T. spegazzinii, almost parallel to the toothrow, but it gradually rises Ameghino, 1909 (Museo Argentino de Ciencias Naturales, posteriorly, as in some young specimens of T. terrestris. Bernardino Rivadavia, Buenos Aires, Argentina [MACN] However, the sagittal crest is lower, shorter, and wider than in 5.41), from Rio Pescado, Departamento de Ora´n, Salta, the latter species. The frontal bones are inflated to form a large Argentina. It has the skull characters of T. terrestris, with a triangular convex exposure, with a longitudinal medial long and high sagittal crest starting in the frontals. depression, ending posteriorly at the frontal–parietal suture, Tapirus terrestris colombianus Hershkovitz, 1954, from El where the sagittal crest begins. In T. terrestris the sagittal crest Salado, eastern slope of Sierra Nevada, department of Magdalena, Colombia, is based on a young adult male skull starts in the frontals, much anteriorly than in T. kabomani. that has all the characteristics of T. terrestris. These features are illustrated in Fig. 4, in comparison with a Consequently, we cannot link any previous names to our skull of T. terrestris. The meatal diverticulum fossae are specimens, and thus we propose a new taxon name. shallower than in the other species, with reduced dorsal Description.—External appearance. For external characters extension. The nasals are similar to those of T. terrestris in we use information from local hunters, who identified the shape and do not project upward, as in T. bairdii and T. animals in the camera-trap photos (Fig. 3) from the type pinchaque. As in all Neotropical species, the maxillary– locality as belonging to the new species. The hair is dark, from premaxillary suture is anterior to the canine. The anteromedial dark gray to dark brownish. The mane, as an external process of the maxilla is dorsal to premaxilla. The rostrum is expression of the sagittal crest, is lower and starts not upturned as in most adults of T. terrestris. posteriorly. The forehead behind the nasals is broader than in Some features show intraspecific variability. The spiral T. terrestris. From the photos, specimens of known sex show grooves in the nasals are shallow in UNIR-M21, AMNH that females have a gray–white area that extends from the 36661, and UFMG 3177, but a little deeper in the holotype. December 2013 COZZUOL ET AL.—NEW AMAZON TAPIR 1337

FIG.5.—Canonical variate analysis scatter-plot for 21 cranial measures of all living Tapirus species and T. rondoniensis. A) All species, B) South American species.

Diastema and rostrum are short in UNIR-M21, but not in scatter-plots (Fig. 5) all species appear clearly separated. The UFMG 3177 and in the holotype. single specimen of T. rondoniensis falls between T. terrestris Morphometrics.—A MANOVA–CVA, including all living and T. kabomani, but out of the range of both of them. species, plus the holotype of T. rondoniensis (Fig. 5A) and then Morphological cladistics.—The morphological cladistic T. kabomani, T. pinchaque, T. terrestris, and T. rondoniensis analysis, which includes all living and selected fossil North (Fig. 5B), was performed. and South American species, results in a single most- In both analyses, T. terrestris discriminates clearly from all parsimonious tree. The genus Tapirus exhibits monophyly. the others with significant discriminant function values, but the The middle to late Miocene species T. johnsoni and the late small sample sizes of the other species preclude the calculation Miocene T. webbi, both from North America, appear as of a discriminant function among them (see Supporting successive clades, the latter is the sister group of the 2 major Information S8, S9, and S10; DOI: 10.1644/ clades, one containing all of the South American species (T. 12-MAMM-A-169.S8, DOI: 10.1644/12-MAMM-A-169.S9, kabomani, T. terrestris, T. pinchaque, T. cristatellus, T. and DOI: 10.1644/12-MAMM-A-169.S10). In the CVA mesopotamicus,andT. rondoniensis)andtheother 1338 JOURNAL OF MAMMALOGY Vol. 94, No. 6

FIG.6.—Morphological maximum-parsimony tree including all living species and selected fossils of Tapirus. The numbers above hash marks correspond to character numbers and, above them, character states. containing the Asian, North American, and Central American be included in the morphological matrix, the position of T. species (T. indicus, T. bairdii, T. polkesnsis, T. haysii, and T. indicus may change in future morphological analyses. veroensis) supported by 2 synapomorphies. The South Genetic evidence.—A total of 960 bp of the Cytb gene, 617 American clade is supported by 5 synapomorphies. T. bp of the COI gene, and 690 bp of COII gene were sequenced mesopotamicus is the sister group of the remaining South for the holotype (UFMG 3177) and 1 paratype (UFMG 3176), American species. T. kabomani appears as the sister taxon of T. and compared with sequences of 64 tapir individuals. Between- rondoniensis, from which it differs by possessing 3 taxa distances for COI, COII, and Cytb data were calculated autapomorphies, whereas T. rondoniensis has 1 using Kimura 2 parameter (Supporting Information S11, S12, autapomorphy. The character distribution in these taxa and S13; DOI: 10.1644/12-MAMM-A-169.S11, DOI: 10. precludes considering these 2 species as synonyms. They are, 1644/12-MAMM-A-169.S12, and DOI: 10.1644/ 12-MAMM-A-169.S13), and reveal a high similarity because in turn, the sister group of a clade including T. terrestris, T. of a close relationship among the 3 South American species. pinchaque, and T. cristatellus (Fig. 6). Bayesian inference and maximum-likelihood phylogenetic The grouping of T. indicus with T. bairdii and several North trees for the Cytb data set were mostly congruent, with small American fossil species is the major difference between discrepancies only in node support (Fig. 7), both having the phylogenetic results of morphological and DNA characters same topology, which also was replicated using the Cytb þ COI (see below). The reason for this is not clear. Because the þ COII data set (Supporting Information S14, DOI: 10.1644/ several fossil species included in the morphological matrix 12-MAMM-A-169.S14). The last one used a smaller sample cannot be assessed genetically, a likely alternative would be a set. The proposed T. kabomani formed a clade with moderate long-branch attraction causing T. bairdii to appear as sister (Cytb, aLRT ¼ 0.55, posterior probability [PP] ¼ 0.73) to taxon of T. indicus in the morphology analysis. Furthermore, strong (all genes combined, aLRT ¼ 0.88, PP ¼ 0.93) support, many other genetic markers have shown T. bairdii as sister sister to T. terrestris and T. pinchaque in all phylogenetic group of the South American tapirs (Steiner and Ryder 2011), reconstructions, involving combined data set (Cytb þ COI þ the same topology we recover in our mtDNA analyses. COII) or only Cytb with a larger sample size. Moreover, a Because no fossil tapirs from Asia are well known enough to similar topology is observed in the maximum-parsimony tree December 2013 COZZUOL ET AL.—NEW AMAZON TAPIR 1339

(figure not shown) and median-joining network analyses (Fig. than the animal I had killed. The hunters said that this was a 8). In all trees, the 2 DNA samples from southeastern distinct kind.’’ Roosevelt sent the specimen to the United States Colombia and 1 on the Brazilian border also were shown to for analysis, but it was considered just a variation of T. belong to the T. kabomani clade (Fig. 7). terrestris (Allen 1914). Tapirus pinchaque presented a well-supported clade, but T. The morphological analysis clearly discriminates T. kabo- terrestris was shown to be paraphyletic with T. pinchaque mani from all other species, particularly from the apparently nested inside it (Fig. 7). T. terrestris appears to be composed of sympatric T. terrestris, with which it has been confused. The at least 5 different clusters (or clades including T. pinchaque) late Pleistocene T. rondoniensis (Holanda et al. 2011), which in the Bayesian inference reconstructions, each supported by comes from close to the type area of T. kabomani, falls PP . 0.99 (aLRT . 0.91 for maximum-likelihood tree). The between T. terrestris and T. kabomani in the CVA, especially restricted and peripheral distribution range of T. pinchaque when only South American species are analyzed (Figs. 5A and suggests it to be the result of a peripatric speciation process. 5B). In the morphological cladogram, T. kabomani is the sister Molecular dating methods (linearized tree and Bayesian taxon of T. rondoniensis, from which it differs by possessing 3 estimation—see ‘‘Materials and Methods’’) indicate a late autapomorphies. Together they are the sister group of the other Miocene to early Pliocene time of divergence of T. bairdii and 2 living South American species. the South American clade (3.16–7.55 mya), and a late Our results concur partially with previous molecular Pleistocene divergence for the T. kabomani and T. terrestris– phylogenies (Norman and Ashley 2000; de Thoisy et al. T. pinchaque complex (288–652 thousand years ago; Fig. 7). 2010; Steiner and Ryder 2011). The mtDNA gene trees (Cytb, The Cytb median-joining network analysis (Fig. 8) support- or Cytb þ COI þ COII) show strong support for a unique ed the basal position of T. kabomani, but also indicated that T. Neotropical clade, encompassing a strict terrestris includes at least 2 main clusters, separated by 6 subclade (Fig. 7). In the Bayesian inference and maximum- mutational steps. T. pinchaque is nested between these 2 likelihood phylogenetic analyses, the T. kabomani clade is clusters (Figs. 7 and 8), 5 steps distant from the larger T. associated with moderate (only Cytb) to strong (Cytb þ COI þ terrestris cluster, and 9 from the smaller one. COII) PP and aLRT values. These results support T. kabomani as a distinctive taxon in a basal position with regard to the other 2 unambiguously recognized South American species (T. DISCUSSION pinchaque and T. terrestris). Morphological and molecular data are in general agreement The oldest record for the genus in South America is about 2 (Figs. 6 and 7; Supporting Information S15, DOI: 10.1644/ mya (Ensenadan South American Land Mammal Age). During 12-MAMM-A-169.S15) and unambiguously identified a new the late Pleistocene the genus attained its largest diversity on well-supported clade among the South American tapirs, the continent (Holanda and Cozzuol 2006), which led to living proposed as Tapirus kabomani sp. nov. species: T. terrestris, T. pinchaque, and T. kabomani. The late Other studies have highlighted the high level of genetic and Pleistocene has been identified of major importance for tapir species diversity among several vertebrate taxa in this region diversification (Hulbert 1999), and more widely for many other (Haffer 1969; Ashley et al. 1996; Avise et al. 1998; Brumfield vertebrate taxa (Haffer 1969; Avise et al. 1998; Brumfield and and Edwards 2007). T. kabomani sp. nov. is an example of Edwards 2007). newly uncovered biodiversity of the Amazon, and shows the Based on knowledge of local peoples and our own congruence of both often-denigrated traditional knowledge observations it appears that the new species is not rare in the with more widely accepted scientific approaches for biodiver- upper Madeira River region, in the southwestern Brazilian sity discovery (Sheil and Lawrance 2004). In a context of Amazon, where mosaics of forest and patches of open savanna global change and accelerated loss of biodiversity, discovery are present, probably Holocene relicts of Cerrado. Where only and description of species should rely on strong and efficient forest or open areas are dominant, the species seems to be rare collaborations with local communities (Pfeiffer and Uril 2003). or absent. If this pattern is confirmed in the future, it may imply Despite technical limits and the obstacle of intellectual property an origin of this species during dry periods of the Pleistocene, that need to be properly managed, the benefits of the associated with forest fragmentation (Haffer 1969; Costa 2003; involvement of local people as ‘‘parataxonomists’’ in biodiver- Mayle 2004; Bonaccorso et al. 2006; Cossios et al. 2009). sity surveys appear indisputable (Janzen et al. 1993; Basset et Fecal samples collected from paths where T. kabomani was al. 2000; Bass et al. 2004; Arias et al. 2012). In the case of a found contained leaves and seeds of the palm trees Atalea newly discovered and already threatened large Neotropical maripa, Orbignya phalerata, and aculeatum. The mammal, local conservation initiatives, as soon as they are also ecology of T. kabomani is otherwise unknown. shared with communities, are more prone to tangible results Southwestern Amazonia is currently undergoing intense (Shanley and Gaia 2002). It is noteworthy that the 1st known landscape modification by and increasing human specimen collected for this species (AMNH 36661) remained population. The region is likely threatened more by global unidentified for almost 100 years although the collector, warming than are other South American regions (Wright et al. Theodore Roosevelt, remarked (Roosevelt 1914: 76) that this 2009), and it is considered a biodiversity hot spot (Haffer 1969; specimen ‘‘. . . was a bull, full grown but very much smaller Harcourt 2000) with undocumented species richness. Particu- 1340 JOURNAL OF MAMMALOGY Vol. 94, No. 6

FIG.7.—A) Bayesian inference phylogenetic tree of cytochrome-b sequences for all tapir species. The same topology was found using a maximum-likelihood approach, excluding identical haplotypes in the analysis. All branches with support statistics , 0.50 were collapsed. Support values shown only for main nodes are approximate likelihood-ratio (aLRT) statistics for maximum-likelihood–Bayesian posterior probabilities. Support values for the Tapirus kabomani (*) and T. pinchaque (**) clades are shown as asterisks. Arrows show nodes where the divergence times were calculated. larly, the state of Rondoˆnia has been the focus of recent human to T. pinchaque than to the other cluster (Fig. 7) and appears to incursion, with high deforestation rates. Large development occur in a restricted geographical region (around Ecuador), the projects are currently underway, such as the construction of 2 2 T. terrestris clusters deserve more attention regarding their large hydroelectric complexes along the upper Madeira River status. Thus, further analysis is needed to assess the variability and the reactivation of the Porto Velho–Manaus highway, BR of T. terrestris (Fig. 8). 319, which will facilitate land occupation in the area where the known specimens were collected. Natural open areas in the RESUMO Amazon have been used for agriculture, which may affect the habitat of the new species. It is thus urgent to determine the Todasasespecies´ conhecidas de antas viventes sa˜o conservation status, geographic range, and environmental alopa´tricas: 1 no sudeste da Asia´ e as 3 na America´ Central requirements of this species, to understand how it is affected eAmerica´ do Sul. Entretanto, o registro fossil´ para antas e´ mais by human activities. amplo geograficamente, incluindo Europa, Asia,´ America´ do Despite discussions about the need for monophyly at species Norte e do Sul, encontrados desde o Oligoceno tardio, tornando level (Funk and Omland 2004), it has been argued that species a distribui¸ca˜o atual um relicto da original. Descrevemos aqui must meet the more restrictive criterion of being genealogically uma nova especie´ de Tapirus vivente da floresta amazoˆnica, a exclusive groups where the members are more closely related primeira desde T. bairdii Gill, 1865, e o primeiro novo to each other than to anything outside the group (Velasco Perissodactyla em mais de 100 anos, a partir de caracteres 2009). Because one T. terrestris cluster is more closely related morfologicos´ e moleculares. O novo ta´xon e´ menor em estatura December 2013 COZZUOL ET AL.—NEW AMAZON TAPIR 1341

FIG.7.—(continued) B) A detail of the above tree showing all branch support values for the South American tapir clade. do que T. terrestris (Linnaeus, 1758) com morfologia distinta Peruana Cayetano Heredia, Lima, Peru), and A. G. Silva (University do cranio,ˆ sendo basal ao clado formado por T. terrestris e T. of British Columbia Okanagan, Kelowna, Canada), who provided pinchaque (Roulin, 1829). Esta descoberta destaca a biodiver- some samples of Neotropical Tapirus (de Thoisy et al. 2010); the San sidade oculta no oeste da Amazoˆnia, onde a biota enfrenta Diego Zoo, San Diego, California, which provided a sample of T. amea¸cas crescentes. Alguns povos locais ha´ muito tempo indicus; L. Avilla (Federal University of the State of Rio de Janeiro, reconheceram esta nova especie,´ sugerindo um papel funda- UNIRIO), who lent us 2 camera-traps; M. Marmontel (Instituto Sustenta´vel Mamiraua´, Tefe,´ Brazil), P. Medici´ (Tapir Specialist mental para o conhecimento tradicional na compreensa˜o da Group, www.tapirs.org), and C. Maria Jacobi (Universidade Federal biodiversidade da regia˜o. de Minas Gerais, Belo Horizonte, Brazil), who helped to improve the manuscript text; and L. Emmons (National Museum of Natural ACKNOWLEDGMENTS History, Smithsonian Institution, Washington, D.C.), who provided This work received grants from Funda¸ca˜o O Botica´rio (FBPN), many comments and English review of the final text. We thank the CNPq, and FAPEMIG from Brazil, and JAGUARS program (funders: biology student G. Braga, who kindly made the life drawings of the Kwata non-governmental organization (NGO), Institut Pasteur de la male and female specimens of T. kabomani in Supporting Information Guyane, and Labex Centre d’Etude de la Biodiversite´ Amazonienne) S6 and S7. of Kwata NGO (www.kwata.net). We thank J. Patton (Museum of Vertebrate Zoology, Berkeley, California) for providing data and SUPPORTING INFORMATION measurements of tapir skulls from his institution, initial comments, and advising on early stage of this manuscript; J. Vianna (Pontificia SUPPORTING INFORMATION S1.—Morphometry. Universidad Catolica´ de Chile, Santiago, Chile) and A. A. Nascimento Found at DOI: 10.1644/12-MAMM-A-169.S1 (Universidade Federal de Minas Gerais, Belo Horizonte, Brazil) for SUPPORTING INFORMATION S2.—List of the specimens used in the participation and discussion in the initial stages of this work; C. morphometric analysis other than Tapirus kabomani. Pedraza (Universidad de Los Andes, Bogota´, Colombia), A. Tapia Found at DOI: 10.1644/12-MAMM-A-169.S2 (Universidad Central del Ecuador, Quito, Ecuador), M. R. Garcia SUPPORTING INFORMATION S3.—Data matrix for the morphological (Universidad Javeriana, Bogota´, Colombia), O. Ramirez (Universidad phylogenetic analysis. 1342 JOURNAL OF MAMMALOGY Vol. 94, No. 6

FIG.8.—Median-joining network of cytochrome-b (Cytb) sequences of Tapirus terrestris, T. kabomani, and T. pinchaque. Numbers of mutational steps larger than 1 are shown for each branch connecting haplotypes. The circle size of each haplotype is proportional to the number of individuals found, and the monophyletic clades belonging to T. kabomani and T. pinchaque are indicated, as well as the out-group root (T. bairdii þ T. indicus). See list of Cytb haplotypes, access numbers, population distribution, and other results for molecular analyses in Supporting Information S5 and S11–S15.

Found at DOI: 10.1644/12-MAMM-A-169.S3 Found at DOI: 10.1644/12-MAMM-A-169.S8 SUPPORTING INFORMATION S4.—Morphological cladistics. SUPPORTING INFORMATION S9.—Multivariate analysis of variance– Found at DOI: 10.1644/12-MAMM-A-169.S4 canonical variate analysis discriminant function for South American SUPPORTING INFORMATION S5.—GenBank accession numbers of species of the genus Tapirus. new sequences generated in this work. Found at DOI: 10.1644/12-MAMM-A-169.S9 Found at DOI: 10.1644/12-MAMM-A-169.S5 SUPPORTING INFORMATION S10.—Jackknifed confusion matrix from SUPPORTING INFORMATION S6.—Pictorial representation of the head the multivariate analysis of variance–canonical variate analysis for of a male Tapirus kabomani. Drawn by Grazielle Braga, UFMG. South American species of the genus Tapirus. Found at DOI: 10.1644/12-MAMM-A-169.S6 Found at DOI: 10.1644/12-MAMM-A-169.S10 SUPPORTING INFORMATION S7.—Pictorial representation of the head SUPPORTING INFORMATION S11.—Between-taxa distances for cyto- of a female Tapirus kabomani. Drawn by Grazielle Braga, UFMG. chrome oxidase I calculated using Kimura 2-parameter models. Found at DOI: 10.1644/12-MAMM-A-169.S7 Found at DOI: 10.1644/12-MAMM-A-169.S11 SUPPORTING INFORMATION S8.—Multivariate analysis of variance– SUPPORTING INFORMATION S12.—Between-taxa distances for cyto- canonical variate analysis discriminant function for all living species chrome oxidase II calculated using Kimura 2-parameter models. of the genus Tapirus. Found at DOI: 10.1644/12-MAMM-A-169.S12 December 2013 COZZUOL ET AL.—NEW AMAZON TAPIR 1343

SUPPORTING INFORMATION S13.—Between-taxa distances for cyto- BLUMENBACH, J. F. 1779. Handbuch der Naturgeschichte. Mit Kupfern. chrome b calculated using Kimura 2-parameter models. Erster Theil, Go¨ttingen, Germany. Found at DOI: 10.1644/12-MAMM-A-169.S13 BONACCORSO, E., L. KOCH, AND A. T. PETERSON. 2006. Pleistocene SUPPORTING INFORMATION S14.—Maximum-likelihood tree for fragmentation of Amazon species’ ranges. Diversity and Distribu- cytochrome b (Cytb) þ cytochrome oxidase I þ cytochrome oxidase tions 12:157–164. II mitochondrial DNA genes. The tree presents the same topology as BRUMFIELD, R. T., AND S. V. EDWARDS. 2007. Evolution into and out of the Bayesian inference tree (not shown), and the taxa grouping reveal the Andes: a Bayesian analysis of historical diversification in about the same branches as shown for the Bayesian inference tree Thamnophilus antshrikes. Evolution 61:346–367. using only Cytb (Fig. 7), without several taxa, including an CEBALLOS, G., AND P. R. EHLRICH. 2009. Discovery of new mammals Ecuadorian Tapirus terrestris branch sister to T. pinchaque. All species and their implications for conservation and ecosystem branches with approximate likelihood-ratios (aLRT) or posterior services. Proceedings of the National Academy of Sciences probabilities (PP) , 0.50 were collapsed. Values are shown for the 106:3841–3846. main branches (aLRT/PP). COSSIOS, D., M. LUCHERINI,M.RUIZ-GARCIA´ , AND B. ANGERS. 2009. Found at DOI: 10.1644/12-MAMM-A-169.S14 Influence of ancient glacial periods on the Andean fauna: the case of SUPPORTING INFORMATION S15.—List of specimens for each the pampas cat (Leopardus colocolo). BMC Evolutionary Biology cytochrome-b haplotype and locality (only for Tapirus terrestris, T. 9:68. pinchaque, and T. kabomani), according the representation in Fig. 8. COSTA, L. P. 2003. 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